fMRI BOLD responses to film stimuli and their association with exhaled nitric oxide in asthma and health

• Published in: Psychophysiology 2024-05, Vol.61 (5), p.e14513-n/a
• Main Authors: Ritz, Thomas, Kroll, Juliet L., Khan, David A., Yezhuvath, Uma S., Aslan, Sina, Pinkham, Amy, Rosenfield, David, Brown, E. Sherwood
• Format: Article
• Language: English
• Subjects: affect; Amygdala; Asthma; Brain mapping; Central nervous system; Cortex (cingulate); Deactivation; exhaled nitric oxide; fMRI; Functional magnetic resonance imaging; Neostriatum; Nitric oxide; partial pressure of carbon dioxide; Periaqueductal gray area; Prefrontal cortex; Ventral tegmentum
• ISSN: 0048-5772; 1469-8986; 1540-5958
• DOI: 10.1111/psyp.14513

Little is known about central nervous system (CNS) responses to emotional stimuli in asthma. Nitric oxide in exhaled breath (FENO) is elevated in asthma due to allergic immune processes, but endogenous nitric oxide is also known to modulate CNS activity. We measured fMRI blood oxygen‐dependent (BOLD) brain activation to negative (blood–injection–injury themes) and neutral films in 31 participants (15 with asthma). Regions‐of‐interest analysis was performed on key areas relevant to central adaptive control, threat processing, or salience networks, with dorsolateral prefrontal cortex (PFC), anterior insula, dorsal anterior cingulate cortex (dACC), amygdala, ventral striatum, ventral tegmentum, and periaqueductal gray, as well as top‐down modulation of emotion, with ventrolateral and ventromedial PFC. Both groups showed less BOLD deactivation from fixation cross‐baseline in the left anterior insula and bilateral ventromedial PFC for negative than neutral films, and for an additional number of areas, including the fusiform gyrus, for film versus recovery phases. Less deactivation during films followed by less recovery from deactivation was found in asthma compared to healthy controls. Changes in PCO2 did not explain these findings. FENO was positively related to BOLD activation in general, but more pronounced in healthy controls and more likely in neutral film processing. Thus, asthma is associated with altered processing of film stimuli across brain regions not limited to central adaptive control, threat processing, or salience networks. Higher levels of NO appear to facilitate CNS activity, but only in healthy controls, possibly due to allergy's masking effects on FENO. Using fMRI and emotion induction by films, this study shows for the first time that individuals with asthma process both affective and neutral stimuli differently at the central nervous system level. Nitric oxide, a vasodilator, measured in exhaled breath, was consistently related to stronger activation across brain areas.